A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization

The symbiosis between reef-building corals and their algal endosymbionts (zooxanthellae of the genus Symbiodinium) is highly sensitive to temperature stress, which makes coral reefs vulnerable to climate change. Thermal tolerance in corals is known to be substantially linked to the type of zooxanthellae they harbour and, when multiple types are present, the relative abundance of types can be experimentally manipulated to increase the thermal limits of individual corals. Although the potential exists for this to translate into substantial thermal acclimatization of coral communities, to date there is no evidence to show that this takes place under natural conditions. In this study, we show field evidence of a dramatic change in the symbiont community of Acropora millepora, a common and widespread Indo-Pacific hard coral species, after a natural bleaching event in early 2006 in the Keppel Islands (Great Barrier Reef). Before bleaching, 93.5% (n=460) of the randomly sampled and tagged colonies predominantly harboured the thermally sensitive Symbiodinium type C2, while the remainder harboured a tolerant Symbiodinium type belonging to clade D or mixtures of C2 and D. After bleaching, 71% of the surviving tagged colonies that were initially C2 predominant changed to D or C1 predominance. Colonies that were originally C2 predominant suffered high mortality (37%) compared with D-predominant colonies (8%). We estimate that just over 18% of the original A. millepora population survived unchanged leaving 29% of the population C2 and 71% D or C1 predominant six months after the bleaching event. This change in the symbiont community structure, while it persists, is likely to have substantially increased the thermal tolerance of this coral population. Understanding the processes that underpin the temporal changes in symbiont communities is key to assessing the acclimatization potential of reef corals.     

Highly hydroxylated or γ-cyclodextrin-bicapped water-soluble derivative of fullerene: The antioxidant ability assessed by electron spin resonance method and β-carotene bleaching assay

Antioxidant ability of the water-soluble derivative of fullerene (C60), prepared by high-degree hydroxylation [C60-(OH)₃₂·8H₂O] or C60/γ-cyclodextrin (1:2 mol/mol) clathrate formation [C60/(γ-CD)₂], was assessed by electron spin resonance method and β-carotene bleaching assay. These C60 derivatives have an ability to diminish a 1:2:2:1 quartet ESR spectrum attributed to hydroxyl radicals (OH) as shown by DMPO-spin trap/ESR method. Meanwhile, a singlet radical-signal different from OH-attributed signals increased in a manner dependent on concentrations of C60-(OH)₃₂·8H₂O. This might suggest that C60-(OH)₃₂·8H₂O scavenges OH owing to dehydrogenation of C60-(OH)₃₂·8H₂O, and is simultaneously oxidized to a stable radical species, which may be a dehydrogenated fullerenol radical (C60-O). Furthermore, these water-soluble derivatives of C60 suppressed fading of yellowish color characteristic of intact β-carotene in β-carotene bleaching assay. Antioxidant abilities of these derivatives were assessed as retention of yellowish color (viz absorbance at 470 nm) for 180 min. Namely, β-carotene-attributed chromaticity (% relative absorbance at 470 nm compared with the control) after 180 min was 69% for C60-(OH)₃₂·8H₂O (400 μM: C60-eq.), and 32% for C60/(γ-CD)₂ (400 μM: C60-eq.), whereas it was 6% for l(+)-ascorbic acid (400 μM) which is hydrophilic, and 85% for (±)-α-tocopherol (400 μM) which is lipophilic, respectively. Thus C60-(OH)₃₂·8H₂O and C60/(γ-CD)₂ can scavenge OH, and have a distinct antioxidative activity in the aqueous system containing linoleic acid which is abundantly contained in the cell membrane together with other unsaturated lipids. These C60 derivatives have a potential to protect the cell membrane from oxidative stress due to OH.     

造礁石珊瑚与其共生藻(Symbiodinium)共生研究进展

对造礁石珊瑚与其共生藻共生研究现状及其在全球变化下的适应能力进行较全面的综述.造礁石珊瑚与遗传和生理功能独特的共生藻组成内共生关系是成功演化的范例.近年来对珊瑚共生体的分子系统学研究表明共生藻遗传多样性极为丰富,当前认为共生藻属至少包括8个(A-H)各自包含亚系群的世系或系群.珊瑚-共生藻共生功能体对诸如全球变化引起的海水温度上升等环境变化十分敏感.由于珊瑚以及珊瑚礁面临气候变化的严峻挑战,对珊瑚与其共生藻共生关系和共生功体适应能力的研究将是未来重要的研究领域之一.     

High zooxanthella density shortens the survival time of coral cell aggregates under thermal stress

To investigate bleaching mechanisms in coral-zooxanthella symbiotic systems, it is important to study the cellular- or tissue-level responses of corals to stress. We established an experimental system to study the stress responses of coral cells using coral cell aggregates. Dissociated coral cells aggregate to form spherical bodies, which rotate by ciliary movement. These spherical bodies (tissue balls) stop rotating and disintegrate when exposed to a thermal stress. Tissue balls prepared from dissociated cells of Fungia sp. and Pavona divaricata were exposed to either elevated temperature (31 °C, with 25 °C as the control) or elevated temperature in the presence of exogenous antioxidants (ascorbic acid and catalase, or mannitol). The survival curves of tissue balls were markedly different between 31 and 25 °C. At 31 °C, most tissue balls disintegrated within 24 h, whereas at 25 °C, most tissue balls survived for more than 24 h. There was a negative correlation between survival time and the zooxanthella density of tissue balls at 31 °C, but no significant relationship was found at 25 °C. Antioxidants extended the survival time of tissue balls at high temperature, suggesting that zooxanthellae produce reactive oxygen species under stress. These results indicate that zooxanthellae produce harmful substances and damage coral cells under high-temperature stress. Tissue balls provide a good experimental system with which to study the effects of stress and various chemical reagents on corals cells.     

Rapid thermal adaptation in photosymbionts of reef‐building corals

Climate warming is occurring at a rate not experienced by life on Earth for 10 s of millions of years, and it is unknown whether the coral‐dinoflagellate (Symbiodinium spp.) symbiosis can evolve fast enough to ensure coral reef persistence. Coral thermal tolerance is partly dependent on the Symbiodinium hosted. Therefore, directed laboratory evolution in Symbiodinium has been proposed as a strategy to enhance coral holobiont thermal tolerance. Using a reciprocal transplant design, we show that the upper temperature tolerance and temperature tolerance range of Symbiodinium C1 increased after ~80 asexual generations (2.5 years) of laboratory thermal selection. Relative to wild‐type cells, selected cells showed superior photophysiological performance and growth rate at 31°C in vitro, and performed no worse at 27°C; they also had lower levels of extracellular reactive oxygen species (exROS). In contrast, wild‐type cells were unable to photosynthesise or grow at 31°C and produced up to 17 times more exROS. In symbiosis, the increased thermal tolerance acquired ex hospite was less apparent. In recruits of two of three species tested, those harbouring selected cells showed no difference in growth between the 27 and 31°C treatments, and a trend of positive growth at both temperatures. Recruits that were inoculated with wild‐type cells, however, showed a significant difference in growth rates between the 27 and 31°C treatments, with a negative growth trend at 31°C. There were no significant differences in the rate and severity of bleaching in coral recruits harbouring wild‐type or selected cells. Our findings highlight the need for additional Symbiodinium genotypes to be tested with this assisted evolution approach. Deciphering the genetic basis of enhanced thermal tolerance in Symbiodinium and the cause behind its limited transference to the coral holobiont in this genotype of Symbiodinium C1 are important next steps for developing methods that aim to increase coral bleaching tolerance.     

Are Niemann‐Pick type C proteins key players in cnidarian–dinoflagellate endosymbioses?

The symbiotic interaction between cnidarians, such as corals and sea anemones, and the unicellular algae Symbiodinium is regulated by yet poorly understood cellular mechanisms, despite the ecological importance of coral reefs. These mechanisms, including host–symbiont recognition and metabolic exchange, control symbiosis stability under normal conditions, but also lead to symbiosis breakdown (bleaching) during stress. This study describes the repertoire of the sterol‐trafficking proteins Niemann‐Pick type C (NPC1 and NPC2) in the symbiotic sea anemone Anemonia viridis. We found one NPC1 gene in contrast to the two genes (NPC1 and NPC1L1) present in vertebrate genomes. While only one NPC2 gene is present in many metazoans, this gene has been duplicated in cnidarians, and we detected four NPC2 genes in A. viridis. However, only one gene (AvNPC2‐d) was upregulated in symbiotic relative to aposymbiotic sea anemones and displayed higher expression in the gastrodermis (symbiont‐containing tissue) than in the epidermis. We performed immunolabelling experiments on tentacle cross sections and demonstrated that the AvNPC2‐d protein was closely associated with symbiosomes. In addition, AvNPC1 and AvNPC2‐d gene expression was strongly downregulated during stress. These data suggest that AvNPC2‐d is involved in both the stability and dysfunction of cnidarian–dinoflagellate symbioses.     

The cumulative impact of annual coral bleaching can turn some coral species winners into losers

Mass coral bleaching events caused by elevated seawater temperatures result in extensive coral loss throughout the tropics, and are projected to increase in frequency and severity. If bleaching becomes an annual event later in this century, more than 90% of coral reefs worldwide may be at risk of long‐term degradation. While corals can recover from single isolated bleaching and can acclimate to recurring bleaching events that are separated by multiple years, it is currently unknown if and how they will survive and possibly acclimatize to annual coral bleaching. Here, we demonstrate for the first time that annual coral bleaching can dramatically alter thermal tolerance in Caribbean corals. We found that high coral energy reserves and changes in the dominant algal endosymbiont type (Symbiodinium spp.) facilitated rapid acclimation in Porites divaricata, whereas low energy reserves and a lack of algal phenotypic plasticity significantly increased susceptibility in Porites astreoides to bleaching the following year. Phenotypic plasticity in the dominant endosymbiont type of Orbicella faveolata did not prevent repeat bleaching, but may have facilitated rapid recovery. Thus, coral holobiont response to an isolated single bleaching event is not an accurate predictor of its response to bleaching the following year. Rather, the cumulative impact of annual coral bleaching can turn some coral species ‘winners’ into ‘losers’, and can also facilitate acclimation and turn some coral species ‘losers’ into ‘winners’. Overall, these findings indicate that cumulative impact of annual coral bleaching could result in some species becoming increasingly susceptible to bleaching and face a long‐term decline, while phenotypically plastic coral species will acclimatize and persist. Thus, annual coral bleaching and recovery could contribute to the selective loss of coral diversity as well as the overall decline of coral reefs in the Caribbean.     

Interaction of cycloheximide and light on chlorophyll content and chloroplast ultrastructure inBrassica campestris

Cycloheximide retarded the loss of chlorophyll from detached komatsuna (Brassica campestris cv. Komatsuna) leaves during incubation in the dark but promoted its loss in light. Cycloheximide-induced chlorophyll bleaching in light was prevented by some active oxygen scavengers. Chloroplast envelopes of cycloheximide-treated leaves incubated in both the dark and light were destroyed within 48 h. The grana of cycloheximide-treated leaves incubated in light were dilated.     

Photointermediates of visual pigments

Much progress has been made in recent years toward understanding the interactions between various proteins responsible for visual transduction which are initiated by an activated state of visual pigments. However, the changes which take place in the visual pigments themselves to convert them to the activated state are more poorly understood. Many spectroscopic techniques have been applied to this problem in recent years and considerable progress has been made. A major goal of these efforts is to understand at which stages protein change occurs and to characterize its structural features. In the visual system evidence is accumulating, for example, that chromophore independent protein change begins immediately prior to lumirhodopsin formation. Considerable insight has been gained recently into the early intermediates of visual transduction and the stage is set to achieve similar understanding of the later intermediates leading to rhodopsin's activated state.     

Thermal refugia against coral bleaching throughout the northern Red Sea

Tropical reefs have been impacted by thermal anomalies caused by global warming that induced coral bleaching and mortality events globally. However, there have only been very few recordings of bleaching within the Red Sea despite covering a latitudinal range of 15° and consequently it has been considered a region that is less sensitive to thermal anomalies. We therefore examined historical patterns of sea surface temperature (SST) and associated anomalies (1982–2012) and compared warming trends with a unique compilation of corresponding coral bleaching records from throughout the region. These data indicated that the northern Red Sea has not experienced mass bleaching despite intensive Degree Heating Weeks (DHW) of >15°C‐weeks. Severe bleaching was restricted to the central and southern Red Sea where DHWs have been more frequent, but far less intense (DHWs <4°C‐weeks). A similar pattern was observed during the 2015–2016 El Niño event during which time corals in the northern Red Sea did not bleach despite high thermal stress (i.e. DHWs >8°C‐weeks), and bleaching was restricted to the central and southern Red Sea despite the lower thermal stress (DHWs < 8°C‐weeks). Heat stress assays carried out in the northern (Hurghada) and central (Thuwal) Red Sea on four key reef‐building species confirmed different regional thermal susceptibility, and that central Red Sea corals are more sensitive to thermal anomalies as compared to those from the north. Together, our data demonstrate that corals in the northern Red Sea have a much higher heat tolerance than their prevailing temperature regime would suggest. In contrast, corals from the central Red Sea are close to their thermal limits, which closely match the maximum annual water temperatures. The northern Red Sea harbours reef‐building corals that live well below their bleaching thresholds and thus we propose that the region represents a thermal refuge of global importance.